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Cited by 48Cellular transport and secretionExtracellular vesicles in diseaseNeuroscience and Neuropharmacology Research

SNARE-Mediated Exocytosis in Neuronal Development

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Urbina, Fabio L., Gupton, Stephanie L.·2020·Frontiers in Molecular Neuroscience
DOI 10.3389/fnmol.2020.00133PMC PMC7427632
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Abstract

The formation of the nervous system involves establishing a complex network of synaptic connections between proper partners. This developmental undertaking requires the rapid expansion of plasma membrane surface area as neurons grow and polarize, extending axons through the extracellular environment. Critical to the expansion of the plasma membrane and addition of plasma membrane material is exocytic vesicle fusion, a regulated mechanism driven by soluble N-ethylmaleimide-sensitive factor attachment proteins receptors (SNAREs). SNARE proteins bring two opposing membranes in close proximity and permit them to fuse, an essential task in eukaryotic cells. Since their discovery, SNAREs have been implicated in a number of critical neuronal functions involving exocytic fusion in addition to synaptic transmission, including neurite initiation and outgrowth, axon specification, axon extension, and synaptogenesis. The number and type of SNAREs critical at each stage of development varies, and decades of research have uncovered a rich variety of SNARE expression and function. The basis of SNARE-mediated fusion, the opening of a fusion pore, remains an enigmatic event, despite an incredible amount of research, as fusion is not only heterogeneous, but also spatially small and temporally fast. Early work led to controversies regarding the fate of the fusion pore after opening, and whether that be dilation or closure. Multiple modes of exocytosis have been proposed, with full-vesicle fusion (FVF) and kiss-and-run (KNR) being the best described. Whereas most in vitro work has reconstituted fusion using VAMP-2, SNAP-25, and syntaxin-1; there is much to learn regarding the behaviors of distinct SNARE complexes. In the past few years, robust heterogeneity in the kinetics and fate of the fusion pore that vary by cell type have been uncovered, suggesting a paradigm shift in how the modes of exocytosis are viewed is warranted. Here, we explore both classic and recent work uncovering the variety of SNAREs and their importance in the development of neurons, as well as historical and newly proposed modes of exocytosis, their regulation, and proteins involved in the regulation of fusion kinetics.

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  • During neuronal morphogenesis, neuronal progenitor cells send out processes that become neurites including a single axon and multiple dendrites.

    “During neuronal morphogenesis, neuronal progenitor cells send out processes that become neurites including a single axon and multiple dendrites (52).”

    From Regulation of cargo exocytosis by a Reps1-Ralbp1-RalA module (2023) · cites this paper as [52]

    The Development of Neurons section says immature neurons extend multiple neurites, one of which becomes an axon while the others acquire dendritic components. It distinguishes those neurons from the neural progenitor cells they were born from; it does not say progenitor cells extend the neurites. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

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  1. Adolfsen B. Saraswati S. Yoshihara M. Troy Littleton J. (2004). Synaptotagmins are trafficked to distinct subcellular domains including the postsynaptic compartment. J. Cell Biol. 166, 249– 260. 10.1083/jcb.200312054 15263020 PMC2172321 · DOI
  2. Advani R. J. Bae H. R. Bock J. B. Chao D. S. Doung Y. C. Prekeris R.. (1998). Seven novel mammalian SNARE proteins localize to distinct membrane compartments. J. Biol. Chem. 273, 10317– 10324. 10.1074/jbc.273.17.10317 9553086 · DOI
  3. Akiyama H. Kamiguchi H. (2015). Second messenger networks for accurate growth cone guidance. Dev. Neurobiol. 75, 411– 422. 10.1002/dneu.22157 24285606 · DOI
  4. Akiyama H. Kamiguchi H. (2010). Phosphatidylinositol 3-kinase facilitates microtubule-dependent membrane transport for neuronal growth cone guidance. J. Biol. Chem. 285, 41740– 41748. 10.1074/jbc.M110.156489 21041312 PMC3009901 · DOI
  5. Albillos A. Dernick G. Horstmann H. Almers W. de Toledo G. A. Lindau M. (1997). The exocytotic event in chromaffin cells revealed by patch amperometry. Nature 389, 509– 512. 10.1038/39081 9333242 · DOI
  6. Anantharam A. Bittner M. A. Aikman R. L. Stuenkel E. L. Schmid S. L. Axelrod D.. (2011). A new role for the dynamin GTPase in the regulation of fusion pore expansion. Mol. Biol. Cell 22, 1907– 1918. 10.1091/mbc.e11-02-0101 21460182 PMC3103406 · DOI
  7. Aravanis A. M. Pyle J. L. Tsien R. W. (2003). Single synaptic vesicles fusing transiently and successively without loss of identity. Nature 423, 643– 647. 10.1038/nature01686 12789339 · DOI
  8. Archer D. A. Graham M. E. Burgoyne R. D. (2002). Complexin regulates the closure of the fusion pore during regulated vesicle exocytosis. J. Biol. Chem. 277, 18249– 18252. 10.1074/jbc.c200166200 11929859 · DOI
  9. Arora S. Saarloos I. Kooistra R. van de Bospoort R. Verhage M. Toonen R. F. (2017). SNAP-25 gene family members differentially support secretory vesicle fusion. J. Cell Sci. 130, 1877– 1889. 10.1242/jcs.201889 28404788 · DOI
  10. Azevedo F. A. C. Carvalho L. R. B. Grinberg L. T. Farfel J. M. Ferretti R. E. L. Leite R. E. P.. (2009). Equal numbers of neuronal and nonneuronal cells make the human brain an isometrically scaled-up primate brain. J. Comp. Neurol. 513, 532– 541. 10.1002/cne.21974 19226510 · DOI · Paper page
  11. Baas P. W. Deitch J. S. Black M. M. Banker G. A. (1988). Polarity orientation of microtubules in hippocampal neurons: uniformity in the axon and nonuniformity in the dendrite. Proc. Natl. Acad. Sci. U S A 85, 8335– 8339. 10.1073/pnas.85.21.8335 3054884 PMC282424 · DOI · Paper page
  12. Balkowiec A. Katz D. M. (2002). Cellular mechanisms regulating activity-dependent release of native brain-derived neurotrophic factor from hippocampal neurons. J. Neurosci. 22, 10399– 10407. 10.1523/jneurosci.22-23-10399.2002 12451139 PMC6758764 · DOI
  13. Bao H. Das D. Courtney N. A. Jiang Y. Briguglio J. S. Lou X.. (2018). Dynamics and number of trans-SNARE complexes determine nascent fusion pore properties. Nature 554, 260– 263. 10.1038/nature25481 29420480 PMC5808578 · DOI
  14. Bello O. D. Auclair S. M. Rothman J. E. Krishnakumar S. S. (2016). Using ApoE nanolipoprotein particles to analyze SNARE-induced fusion pores. Langmuir 32, 3015– 3023. 10.1021/acs.langmuir.6b00245 26972604 PMC4946868 · DOI
  15. Bilimoria P. M. Bonni A. (2013). Molecular control of axon branching. Neuroscientist 19, 16– 24. 10.1177/1073858411426201 22179123 PMC3490022 · DOI
  16. Block M. R. Glick B. S. Wilcox C. A. Wieland F. T. Rothman J. E. (1988). Purification of an N-ethylmaleimide-sensitive protein catalyzing vesicular transport. Proc. Natl. Acad. Sci. 85, 7852– 7856. 10.1073/pnas.85.21.7852 3186695 PMC282295 · DOI
  17. Bock J. B. Klumperman J. Davanger S. Scheller R. H. (1997). Syntaxin 6 functions in trans-Golgi network vesicle trafficking. Mol. Biol. Cell 8, 1261– 1271. 10.1091/mbc.8.7.1261 9243506 PMC276151 · DOI
  18. Bock J. B. Matern H. T. Peden A. A. Scheller R. H. (2001). A genomic perspective on membrane compartment organization. Nature 409, 839– 841. 10.1038/35057024 11237004 · DOI
  19. Bowser D. N. Khakh B. S. (2007). Two forms of single-vesicle astrocyte exocytosis imaged with total internal reflection fluorescence microscopy. Proc. Natl. Acad. Sci. U S A 104, 4212– 4217. 10.1073/pnas.0607625104 17360502 PMC1820734 · DOI
  20. Bradke F. Dotti C. G. (1997). Neuronal polarity: vectorial cytoplasmic flow precedes axon formation. Neuron 19, 1175– 1186. 10.1016/s0896-6273(00)80410-9 9427242 · DOI
  21. Bray D. (1970). Surface movements during the growth of single explanted neurons. Proc. Natl. Acad. Sci. U S A 65, 905– 910. 10.1073/pnas.65.4.905 5266160 PMC283002 · DOI
  22. Bretou M. Jouannot O. Fanget I. Pierobon P. Larochette N. Gestraud P.. (2014). Cdc42 controls the dilation of the exocytotic fusion pore by regulating membrane tension. Mol. Biol. Cell 25, 3195– 3209. 10.1091/mbc.e14-07-1229 25143404 PMC4196869 · DOI
  23. Burgo A. Proux-Gillardeaux V. Sotirakis E. Bun P. Casano A. Verraes A.. (2012). A molecular network for the transport of the TI-VAMP/VAMP7 vesicles from cell center to periphery. Dev. Cell 23, 166– 180. 10.1016/j.devcel.2012.04.019 22705394 · DOI
  24. Cardoso-Moreira M. Halbert J. Valloton D. Velten B. Chen C. Shao Y.. (2019). Gene expression across mammalian organ development. Nature 571, 505– 509. 10.1038/s41586-019-1338-5 31243369 PMC6658352 · DOI · Paper page
  25. Ceccarelli B. Hurlbut W. P. Mauro A. (1972). Depletion of vesicles from frog neuromuscular junctions by prolonged tetanic stimulation. J. Cell Biol. 54, 30– 38. 10.1083/jcb.54.1.30 4338962 PMC2108853 · DOI
  26. Chapman E. R. (2008). How does synaptotagmin trigger neurotransmitter release? Annu. Rev. Biochem. 77, 615– 641. 10.1146/annurev.biochem.77.062005.101135 18275379 · DOI
  27. Cheng J. Liu W. Duffney L. J. Yan Z. (2013). SNARE proteins are essential in the potentiation of NMDA receptors by group II metabotropic glutamate receptors. J. Physiol. 591, 3935– 3947. 10.1113/jphysiol.2013.255075 23774277 PMC3764638 · DOI
  28. Clary D. O. Griff I. C. Rothman J. E. (1990). SNAPs, a family of NSF attachment proteins involved in intracellular membrane fusion in animals and yeast. Cell 61, 709– 721. 10.1016/0092-8674(90)90482-t 2111733 · DOI
  29. Cooper J. A. (2013). Mechanisms of cell migration in the nervous system. J. Cell Biol. 202, 725– 734. 10.1083/jcb.201305021 23999166 PMC3760606 · DOI
  30. Cotrufo T. Andrés R. M. Ros O. Pérez-Brangulí F. Muhaisen A. Fuschini G.. (2012). Syntaxin 1 is required for DCC/Netrin-1-dependent chemoattraction of migrating neurons from the lower rhombic lip. Eur. J. Neurosci. 36, 3152– 3164. 10.1111/j.1460-9568.2012.08259.x 22946563 · DOI
  31. Craig A. M. Wyborski R. J. Banker G. (1995). Preferential addition of newly synthesized membrane protein at axonal growth cones. Nature 375, 592– 594. 10.1038/375592a0 7791876 · DOI
  32. Crary J. L. Haldar K. (1992). Brefeldin A inhibits protein secretion and parasite maturation in the ring stage of Plasmodium falciparum. Mol. Biochem. Parasitol. 53, 185– 192. 10.1016/0166-6851(92)90020-k 1501638 · DOI
  33. Diz-Muñoz A. Fletcher D. A. Weiner O. D. (2013). Use the force: membrane tension as an organizer of cell shape and motility. Trends Cell Biol. 23, 47– 53. 10.1016/j.tcb.2012.09.006 23122885 PMC3558607 · DOI
  34. Dotti C. G. Sullivan C. A. Banker G. A. (1988). The establishment of polarity by hippocampal neurons in culture. J. Neurosci. 8, 1454– 1468. 10.1523/jneurosci.08-04-01454.1988 3282038 PMC6569279 · DOI · Paper page
  35. Drachman D. A. (2005). Do we have brain to spare? Neurology 64, 2004– 2005. 10.1212/01.wnl.0000166914.38327.bb 15985565 · DOI
  36. Dudanova I. Klein R. (2013). Integration of guidance cues: parallel signaling and crosstalk. Trends Neurosci. 36, 295– 304. 10.1016/j.tins.2013.01.007 23485451 · DOI
  37. Fasshauer D. Sutton R. B. Brunger A. T. Jahn R. (1998). Conserved structural features of the synaptic fusion complex: SNARE proteins reclassified as Q- and R-SNAREs. Proc. Natl. Acad. Sci. 95, 15781– 15786. 10.1073/pnas.95.26.15781 9861047 PMC28121 · DOI
  38. Fernandez J. M. Neher E. Gomperts B. D. (1984). Capacitance measurements reveal stepwise fusion events in degranulating mast cells. Nature 312, 453– 455. 10.1038/312453a0 6504157 · DOI
  39. Frischknecht R. Fejtova A. Viesti M. Stephan A. Sonderegger P. (2008). Activity-induced synaptic capture and exocytosis of the neuronal serine protease neurotrypsin. J. Neurosci. 28, 1568– 1579. 10.1523/jneurosci.3398-07.2008 18272678 PMC6671550 · DOI
  40. Frühbeis C. Fröhlich D. Kuo W. P. Amphornrat J. Thilemann S. Saab A. S.. (2013). Neurotransmitter-triggered transfer of exosomes mediates oligodendrocyte-neuron communication. PLoS Biol. 11: e1001604. 10.1371/journal.pbio.1001604 23874151 PMC3706306 · DOI · Paper page
  41. Gandhi S. P. Stevens C. F. (2003). Three modes of synaptic vesicular recycling revealed by single-vesicle imaging. Nature 423, 607– 613. 10.1038/nature01677 12789331 · DOI
  42. Gao Y. Zorman S. Gundersen G. Xi Z. Ma L. Sirinakis G.. (2012). Single reconstituted neuronal SNARE complexes zipper in three distinct stages. Science 337, 1340– 1343. 10.1126/science.1224492 22903523 PMC3677750 · DOI
  43. Gasman S. Chasserot-Golaz S. Malacombe M. Way M. Bader M.-F. (2004). Regulated exocytosis in neuroendocrine cells: a role for subplasmalemmal Cdc42/N-WASP-induced actin filaments. Mol. Biol. Cell 15, 520– 531. 10.1091/mbc.e03-06-0402 14617808 PMC329227 · DOI
  44. Gauthier N. C. Fardin M. A. Roca-Cusachs P. Sheetz M. P. (2011). Temporary increase in plasma membrane tension coordinates the activation of exocytosis and contraction during cell spreading. Proc. Natl. Acad. Sci. U S A 108, 14467– 14472. 10.1073/pnas.1105845108 21808040 PMC3167546 · DOI
  45. Gomez T. M. Zheng J. Q. (2006). The molecular basis for calcium-dependent axon pathfinding. Nat. Rev. Neurosci. 7, 115– 125. 10.1038/nrn1844 16429121 · DOI · Paper page
  46. González-Jamett A. M. Momboisse F. Guerra M. J. Ory S. Báez-Matus X. Barraza N.. (2013). Dynamin-2 regulates fusion pore expansion and quantal release through a mechanism that involves actin dynamics in neuroendocrine chromaffin cells. PLoS One 8: e70638. 10.1371/journal.pone.0070638 23940613 PMC3734226 · DOI
  47. Grafmüller A. Shillcock J. Lipowsky R. (2009). The fusion of membranes and vesicles: pathway and energy barriers from dissipative particle dynamics. Biophys. J. 96, 2658– 2675. 10.1016/j.bpj.2008.11.073 19348749 PMC2711276 · DOI
  48. Grassi D. Plonka F. B. Oksdath M. Guil A. N. Sosa L. J. Quiroga S. (2015). Selected SNARE proteins are essential for the polarized membrane insertion of igf-1 receptor and the regulation of initial axonal outgrowth in neurons. Cell Discov. 1: 15023. 10.1038/celldisc.2015.23 27462422 PMC4860833 · DOI
  49. Gupton S. L. Gertler F. B. (2010). Integrin signaling switches the cytoskeletal and exocytic machinery that drives neuritogenesis. Dev. Cell 18, 725– 736. 10.1016/j.devcel.2010.02.017 20493807 PMC3383070 · DOI
  50. Harata N. C. Choi S. Pyle J. L. Aravanis A. M. Tsien R. W. (2006). Frequency-dependent kinetics and prevalence of kiss-and-run and reuse at hippocampal synapses studied with novel quenching methods. Neuron 49, 243– 256. 10.1016/j.neuron.2005.12.018 16423698 · DOI
  51. Hartmann M. Heumann R. Lessmann V. (2001). Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J. 20, 5887– 5897. 10.1093/emboj/20.21.5887 11689429 PMC125691 · DOI
  52. Heuser J. E. (1989). Review of electron microscopic evidence favouring vesicle exocytosis as the structural basis for quantal release during synaptic transmission. Q. J. Exp. Physiol. 74, 1051– 1069. 10.1113/expphysiol.1989.sp003333 2560556 · DOI
  53. Heuser J. E. Reese T. S. (1973). Evidence for recycling of synaptic vesicle membrane during transmitter release at the frog neuromuscular junction. J. Cell Biol. 57, 315– 344. 10.1083/jcb.57.2.315 4348786 PMC2108984 · DOI
  54. Hirling H. Steiner P. Chaperon C. Marsault R. Regazzi R. Catsicas S. (2000). Syntaxin 13 is a developmentally regulated SNARE involved in neurite outgrowth and endosomal trafficking. Eur. J. Neurosci. 12, 1913– 1923. 10.1046/j.1460-9568.2000.00076.x 10886332 · DOI
  55. Holt M. Varoqueaux F. Wiederhold K. Takamori S. Urlaub H. Fasshauer D.. (2006). Identification of SNAP-47, a novel Qbc-SNARE with ubiquitous expression. J. Biol. Chem. 281, 17076– 17083. 10.3410/f.1033038.375051 16621800 · DOI
  56. Horton A. C. Rácz B. Monson E. E. Lin A. L. Weinberg R. J. Ehlers M. D. (2005). Polarized secretory trafficking directs cargo for asymmetric dendrite growth and morphogenesis. Neuron 48, 757– 771. 10.1016/j.neuron.2005.11.005 16337914 · DOI
  57. Hu C. Ahmed M. Melia T. J. Söllner T. H. Mayer T. Rothman J. E. (2003). Fusion of cells by flipped SNAREs. Science 300, 1745– 1749. 10.1126/science.1084909 12805548 · DOI
  58. Hunt D. L. Castillo P. E. (2012). Synaptic plasticity of NMDA receptors: mechanisms and functional implications. Curr. Opin. Neurobiol. 22, 496– 508. 10.1016/j.conb.2012.01.007 22325859 PMC3482462 · DOI
  59. Igarashi M. Kozaki S. Terakawa S. Kawano S. Ide C. Komiya Y. (1996). Growth cone collapse and inhibition of neurite growth by Botulinum neurotoxin C1: a t-SNARE is involved in axonal growth. J. Cell Biol. 134, 205– 215. 10.1083/jcb.134.1.205 8698815 PMC2120926 · DOI
  60. Igarashi M. Tagaya M. Komiya Y. (1997). The soluble N-ethylmaleimide-sensitive factor attached protein receptor complex in growth cones: molecular aspects of the axon terminal development. J. Neurosci. 17, 1460– 1470. 10.1523/jneurosci.17-04-01460.1997 9006987 PMC6793737 · DOI
  61. Jackson J. Papadopulos A. Meunier F. A. McCluskey A. Robinson P. J. Keating D. J. (2015). Small molecules demonstrate the role of dynamin as a bi-directional regulator of the exocytosis fusion pore and vesicle release. Mol. Psychiatry 20, 810– 819. 10.1038/mp.2015.56 25939402 · DOI
  62. Jahn R. Fasshauer D. (2012). Molecular machines governing exocytosis of synaptic vesicles. Nature 490, 201– 207. 10.1038/nature11320 23060190 PMC4461657 · DOI
  63. Jung J.-J. Inamdar S. M. Tiwari A. Choudhury A. (2012). Regulation of intracellular membrane trafficking and cell dynamics by syntaxin-6. Biosci. Rep. 32, 383– 391. 10.1042/bsr20120006 22489884 PMC3392101 · DOI
  64. Kabayama H. Tokushige N. Takeuchi M. Mikoshiba K. (2008). Syntaxin 6 regulates nerve growth factor-dependent neurite outgrowth. Neurosci. Lett. 436, 340– 344. 10.1016/j.neulet.2008.03.061 18406529 · DOI
  65. Kaibuchi K. (2009). Neuronal polarity: from extracellular signals to intracellular mechanisms. Neurosci. Res. 65: S2. 10.1016/j.neures.2009.09.013 17311006 · DOI
  66. Kloepper T. H. Nickias Kienle C. Fasshauer D. (2007). An elaborate classification of SNARE proteins sheds light on the conservation of the eukaryotic endomembrane system. Mol. Biol. Cell 18, 3463– 3471. 10.1091/mbc.e07-03-0193 17596510 PMC1951749 · DOI
  67. Kusumi A. Nakada C. Ritchie K. Murase K. Suzuki K. Murakoshi H.. (2005). Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu. Rev. Biophys. Biomol. Struct. 34, 351– 378. 10.1146/annurev.biophys.34.040204.144637 15869394 · DOI
  68. Le N. Q. K. Huynh T.-T. (2019). Identifying SNAREs by incorporating deep learning architecture and amino acid embedding representation. Front. Physiol. 10: 1501. 10.3389/fphys.2019.01501 31920706 PMC6914855 · DOI
  69. Le N. Q. K. Nguyen V.-N. (2019). SNARE-CNN: a 2D convolutional neural network architecture to identify SNARE proteins from high-throughput sequencing data. PeerJ Comput. Sci. 5: e177 10.7287/peerj-cs.177v0.1/reviews/1 PMC7924420 33816830 · DOI
  70. Lewis S. (2013). Transporting cargo from A to B. Nat. Rev. Neurosci. 14, 589– 589. 10.1038/nrn3568 23900413 · DOI
  71. Liu W. Montana V. Bai J. Chapman E. R. Mohideen U. Parpura V. (2006). Single molecule mechanical probing of the SNARE protein interactions. Biophys. J. 91, 744– 758. 10.1529/biophysj.105.073312 16648158 PMC1483094 · DOI
  72. Logan T. Bendor J. Toupin C. Thorn K. Edwards R. H. (2017). α-synuclein promotes dilation of the exocytotic fusion pore. Nat‥ Neurosci. 20, 681– 689. 10.1038/nn.4529 28288128 PMC5404982 · DOI
  73. Lu X. Zhang F. McNew J. A. Shin Y.-K. (2005). Membrane fusion induced by neuronal SNAREs transits through hemifusion. J. Biol. Chem. 280, 30538– 30541. 10.1074/jbc.m506862200 15980065 · DOI
  74. Lundberg J. M. Rudehill A. Sollevi A. Theodorsson-Norheim E. Hamberger B. (1986). Frequency- and reserpine-dependent chemical coding of sympathetic transmission: differential release of noradrenaline and neuropeptide Y from pig spleen. Neurosci. Lett. 63, 96– 100. 10.1016/0304-3940(86)90020-0 3005926 · DOI
  75. Lüscher C. Isaac J. T. (2009). The synapse: center stage for many brain diseases. J. Physiol. 587, 727– 729. 10.1113/jphysiol.2008.167742 19074963 PMC2669966 · DOI
  76. Malhotra V. (1988). Role of an N-ethylmaleimide-sensitive transport component in promoting fusion of transport vesicles with cisternae of the Golgi stack. Cell 54, 221– 227. 10.1016/0092-8674(88)90554-5 3390865 · DOI
  77. Martinez-Arca S. Coco S. Mainguy G. Schenk U. Alberts P. Bouillé P.. (2001). A common exocytotic mechanism mediates axonal and dendritic outgrowth. J. Neurosci. 21, 3830– 3838. 10.1523/JNEUROSCI.21-11-03830.2001 11356871 PMC6762683 · DOI
  78. McDargh Z. A. Polley A. O’Shaughnessy B. (2018). SNARE-mediated membrane fusion is a two-stage process driven by entropic forces. FEBS Lett. 592, 3504– 3515. 10.1002/1873-3468.13277 30346036 PMC6298751 · DOI
  79. Merighi A. (2018). Costorage of high molecular weight neurotransmitters in large dense core vesicles of mammalian neurons. Front. Cell. Neurosci. 12: 272. 10.3389/fncel.2018.00272 30186121 PMC6110924 · DOI
  80. Micheva K. D. Busse B. Weiler N. C. O’Rourke N. Smith S. J. (2010). Single-synapse analysis of a diverse synapse population: proteomic imaging methods and markers. Neuron 68, 639– 653. 10.1016/j.neuron.2010.09.024 21092855 PMC2995697 · DOI
  81. Miesenböck G. De Angelis D. A. Rothman J. E. (1998). Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394, 192– 195. 10.1038/28190 9671304 · DOI
  82. Min D. Kim K. Hyeon C. Cho Y. H. Shin Y.-K. Yoon T.-Y. (2013). Mechanical unzipping and rezipping of a single SNARE complex reveals hysteresis as a force-generating mechanism. Nat. Commun. 4: 1705. 10.1038/ncomms2692 23591872 PMC3644077 · DOI
  83. Molnár Z. López-Bendito G. Small J. Partridge L. D. Blakemore C. Wilson M. C. (2002). Normal development of embryonic thalamocortical connectivity in the absence of evoked synaptic activity. J. Neurosci. 22, 10313– 10323. 10.1523/jneurosci.22-23-10313.2002 12451131 PMC6758728 · DOI
  84. Mostafavi H. Thiyagarajan S. Stratton B. S. Karatekin E. Warner J. M. Rothman J. E.. (2017). Entropic forces drive self-organization and membrane fusion by SNARE proteins. Proc. Natl. Acad. Sci. U S A 114, 5455– 5460. 10.1073/pnas.1611506114 28490503 PMC5448213 · DOI
  85. Mouritsen O. G. Bloom M. (1984). Mattress model of lipid-protein interactions in membranes. Biophys. J. 46, 141– 153. 10.1016/s0006-3495(84)84007-2 6478029 PMC1435039 · DOI
  86. Mullock B. M. Smith C. W. Ihrke G. Bright N. A. Lindsay M. Parkinson E. J.. (2000). Syntaxin 7 is localized to late endosome compartments, associates with Vamp 8 and Is required for late endosome-lysosome fusion. Mol. Biol. Cell 11, 3137– 3153. 10.1091/mbc.11.9.3137 10982406 PMC14981 · DOI
  87. Nath V. R. Mishra S. Basak B. Trivedi D. Raghu P. (2019). Extended synaptotagmin regulates plasma membrane-endoplasmic reticulum contact site structure and lipid transfer function in vivo. bioRxiv [Preprint]. 10.1101/2019.12.12.874933 PMC7507014 32716137 · DOI
  88. Novick P. Schekman R. (1979). Secretion and cell-surface growth are blocked in a temperature-sensitive mutant of Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. 76, 1858– 1862. 10.1073/pnas.76.4.1858 377286 PMC383491 · DOI
  89. Osen-Sand A. Staple J. K. Naldi E. Schiavo G. Rossetto O. Petitpierre S.. (1996). Common and distinct fusion proteins in axonal growth and transmitter release. J. Comp. Neurol. 367, 222– 234. 8708006
  90. Parlati F. McNew J. A. Fukuda R. Miller R. Söllner T. H. Rothman J. E. (2000). Topological restriction of SNARE-dependent membrane fusion. Nature 407, 194– 198. 10.1038/35025076 11001058 · DOI
  91. Parlati F. Varlamov O. Paz K. McNew J. A. Hurtado D. Söllner T. H.. (2002). Distinct SNARE complexes mediating membrane fusion in Golgi transport based on combinatorial specificity. Proc. Natl. Acad. Sci. U S A 99, 5424– 5429. 10.1073/pnas.082100899 11959998 PMC122785 · DOI
  92. Pfenninger K. H. (2009). Plasma membrane expansion: a neuron’s Herculean task. Nat. Rev. Neurosci. 10, 251– 261. 10.1038/nrn2593 19259102 · DOI
  93. Pfenninger K. H. Friedman L. B. (1993). Sites of plasmalemmal expansion in growth cones. Brain Res. Dev. Brain Res. 71, 181– 192. 10.1016/0165-3806(93)90170-f 8491040 · DOI
  94. Popov S. Brown A. Poo M. (1993). Forward plasma membrane flow in growing nerve processes. Science 259, 244– 246. 10.1126/science.7678471 7678471 · DOI
  95. Prekeris R. Yang B. Oorschot V. Klumperman J. Scheller R. H. (1999). Differential roles of syntaxin 7 and syntaxin 8 in endosomal trafficking. Mol. Biol. Cell 10, 3891– 3908. 10.1091/mbc.10.11.3891 10564279 PMC25687 · DOI
  96. Qu L. Akbergenova Y. Hu Y. Schikorski T. (2009). Synapse-to-synapse variation in mean synaptic vesicle size and its relationship with synaptic morphology and function. J. Comp. Neurol. 514, 343– 352. 10.1002/cne.22007 19330815 · DOI
  97. Rao T. C. Rodriguez Z. S. Bradberry M. M. Ranski A. H. Dahl P. J. Schmidtke M. W.. (2017). Synaptotagmin isoforms confer distinct activation kinetics and dynamics to chromaffin cell granules. J. Gen. Physiol. 149, 763– 780. 10.1085/jgp.201711757 28687607 PMC5560776 · DOI
  98. Richards D. A. (2009). Vesicular release mode shapes the postsynaptic response at hippocampal synapses. J. Physiol. 587, 5073– 5080. 10.1113/jphysiol.2009.175315 19752123 PMC2790249 · DOI
  99. Risselada H. J. Smirnova Y. Grubmüller H. (2014). Free energy landscape of rim-pore expansion in membrane fusion. Biophys. J. 107, 2287– 2295. 10.1016/j.bpj.2014.08.022 25418297 PMC4241460 · DOI
  100. Rizzoli S. O. Jahn R. (2007). Kiss-and-run, collapse and “readily retrievable” vesicles. Traffic 8, 1137– 1144. 10.1111/j.1600-0854.2007.00614.x 17645434 · DOI
  101. Ros O. Cotrufo T. Martínez-Mármol R. Soriano E. (2015). Regulation of patterned dynamics of local exocytosis in growth cones by netrin-1. J. Neurosci. 35, 5156– 5170. 10.1523/JNEUROSCI.0124-14.2015 25834042 PMC6705414 · DOI
  102. Rothman J. E. Orci L. (1992). Molecular dissection of the secretory pathway. Nature 355, 409– 415. 10.1038/355409a0 1734280 · DOI
  103. Sabo S. L. McAllister A. K. (2003). Mobility and cycling of synaptic protein-containing vesicles in axonal growth cone filopodia. Nat. Neurosci. 6, 1264– 1269. 10.1038/nn1149 14608359 · DOI
  104. Sampo B. Kaech S. Kunz S. Banker G. (2003). Two distinct mechanisms target membrane proteins to the axonal surface. Neuron 37, 611– 624. 10.1016/s0896-6273(03)00058-8 12597859 · DOI
  105. Schoch S. Deák F. Königstorfer A. Mozhayeva M. Sara Y. Südhof T. C.. (2001). SNARE function analyzed in synaptobrevin/VAMP knockout mice. Science 294, 1117– 1122. 10.1126/science.1064335 11691998 · DOI
  106. Schulz J. B. Hausmann L. (2016). Synaptopathies: synaptic dysfunction in neurological disorders—a review written by students for students and a story of success for ISN schools. J. Neurochem. 138, 783– 784. 10.1111/jnc.13755 27604179 · DOI
  107. Shah N. Klausner R. D. (1993). Brefeldin A reversibly inhibits secretion in Saccharomyces cerevisiae. J. Biol. Chem. 268, 5345– 5348. 8449896
  108. Shi L. Shen Q.-T. Kiel A. Wang J. Wang H.-W. Melia T. J.. (2012). SNARE proteins: one to fuse and three to keep the nascent fusion pore open. Science 335, 1355– 1359. 10.1126/science.1214984 22422984 PMC3736847 · DOI
  109. Shimojo M. Courchet J. Pieraut S. Torabi-Rander N. Sando R. 3rd Polleux F.. (2015). SNAREs controlling vesicular release of BDNF and development of callosal axons. Cell Rep. 11, 1054– 1066. 10.1016/j.celrep.2015.04.032 25959820 PMC4439258 · DOI
  110. Shin W. Arpino G. Thiyagarajan S. Su R. Ge L. McDargh Z.. (2020). Vesicle shrinking and enlargement play opposing roles in the release of exocytotic contents. Cell Rep. 30, 421.e7– 431.e7. 10.1016/j.celrep.2019.12.044 31940486 PMC7010319 · DOI
  111. Shin W. Ge L. Arpino G. Villarreal S. A. Hamid E. Liu H.. (2018). Visualization of membrane pore in live cells reveals a dynamic-pore theory governing fusion and endocytosis. Cell 173, 934.e12– 945.e12. 10.1016/j.cell.2018.02.062 29606354 PMC5935532 · DOI
  112. Söllner T. Whiteheart S. W. Brunner M. Erdjument-Bromage H. Geromanos S. Tempst P.. (1993). SNAP receptors implicated in vesicle targeting and fusion. Nature 362, 318– 324. 10.1038/362318a0 8455717 · DOI
  113. Sosa L. Dupraz S. Laurino L. Bollati F. Bisbal M. Cáceres A.. (2006). IGF-1 receptor is essential for the establishment of hippocampal neuronal polarity. Nat. Neurosci. 9, 993– 995. 10.1038/nn1742 16845384 · DOI
  114. Sperotto M. M. Ipsen J. H. Mouritsen O. G. (1989). Theory of protein-induced lateral phase separation in lipid membranes. Cell Biophys. 14, 79– 95. 10.1007/bf02797393 2465088 · DOI
  115. Staal R. G. W. Mosharov E. V. Sulzer D. (2004). Dopamine neurons release transmitter via a flickering fusion pore. Nat. Neurosci. 7, 341– 346. 10.1038/nn1205 14990933 · DOI
  116. Steegmaier M. Klumperman J. Foletti D. L. Yoo J.-S. Scheller R. H. (1999). Vesicle-associated membrane protein 4 is implicated in trans-golgi network vesicle trafficking. Mol. Biol. Cell 10, 1957– 1972. 10.1091/mbc.10.6.1957 10359608 PMC25394 · DOI
  117. Steegmaier M. Yang B. Yoo J. S. Huang B. Shen M. Yu S.. (1998). Three novel proteins of the syntaxin/SNAP-25 family. J. Biol. Chem. 273, 34171– 34179. 10.1074/jbc.273.51.34171 9852078 · DOI
  118. Steinman R. M. Mellman I. S. Muller W. A. Cohn Z. A. (1983). Endocytosis and the recycling of plasma membrane. J. Cell Biol. 96, 1– 27. 10.1083/jcb.96.1.1 6298247 PMC2112240 · DOI
  119. Stepanova T. Slemmer J. Hoogenraad C. C. Lansbergen G. Dortland B. De Zeeuw C. I.. (2003). Visualization of microtubule growth in cultured neurons via the use of EB3-GFP (end-binding protein 3-green fluorescent protein). J. Neurosci. 23, 2655– 2664. 10.1523/JNEUROSCI.23-07-02655.2003 12684451 PMC6742099 · DOI
  120. Stevens C. F. Williams J. H. (2000). “Kiss and run” exocytosis at hippocampal synapses. Proc. Natl. Acad. Sci. 97, 12828– 12833. 10.1073/pnas.230438697 11050187 PMC18849 · DOI
  121. Stratton B. S. Warner J. M. Wu Z. Nikolaus J. Wei G. Wagnon E.. (2016). Cholesterol increases the openness of SNARE-mediated flickering fusion pores. Biophys. J. 110, 1538– 1550. 10.1016/j.bpj.2016.02.019 27074679 PMC4833774 · DOI
  122. Südhof T. C. (2004). The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509– 547. 10.1146/annurev.neuro.26.041002.131412 15217342 · DOI · Paper page
  123. Südhof T. C. Rothman J. E. (2009). Membrane fusion: grappling with SNARE and SM proteins. Science 323, 474– 477. 10.1126/science.1161748 19164740 PMC3736821 · DOI · Paper page
  124. Sutherland D. J. Pujic Z. Goodhill G. J. (2014). Calcium signaling in axon guidance. Trends Neurosci. 37, 424– 432. 10.1016/j.tins.2014.05.008 24969461 · DOI
  125. Tojima T. (2012). Intracellular signaling and membrane trafficking control bidirectional growth cone guidance. Neurosci. Res. 73, 269– 274. 10.1016/j.neures.2012.05.010 22684022 · DOI
  126. Tojima T. Akiyama H. Itofusa R. Li Y. Katayama H. Miyawaki A.. (2007). Attractive axon guidance involves asymmetric membrane transport and exocytosis in the growth cone. Nat. Neurosci. 10, 58– 66. 10.1038/nn1814 17159991 · DOI
  127. Tojima T. Hines J. H. Henley J. R. Kamiguchi H. (2011). Second messengers and membrane trafficking direct and organize growth cone steering. Nat. Rev. Neurosci. 12, 191– 203. 10.1038/nrn2996 21386859 PMC3133775 · DOI
  128. Tojima T. Kamiguchi H. (2015). Exocytic and endocytic membrane trafficking in axon development. Dev. Growth Diff. 57, 291– 304. 10.1111/dgd.12218 25966925 · DOI
  129. Torregrosa-Hetland C. J. Villanueva J. Garcia-Martínez V. Expósito-Romero G. Francés M. D. M. Gutiérrez L. M. (2013). Cortical F-actin affects the localization and dynamics of SNAP-25 membrane clusters in chromaffin cells. Int. J. Biochem. Cell Biol. 45, 583– 592. 10.1016/j.biocel.2012.11.021 23220175 · DOI
  130. Urbina F. L. Gomez S. M. Gupton S. L. (2018). Spatiotemporal organization of exocytosis emerges during neuronal shape change. J. Cell Biol. 217, 1113– 1128. 10.1083/jcb.201709064 29351997 PMC5839795 · DOI
  131. Urbina F. L. Menon S. Goldfarb D. Edwards R. Major M. B. Brennwald P. (2020). TRIM67 regulates exocytic mode and neuronal morphogenesis via SNAP47. bioRxiv [Preprint]. 10.1101/2020.02.01.930404 PMC7941186 33567284 · DOI
  132. Washbourne P. Thompson P. M. Carta M. Costa E. T. Mathews J. R. Lopez-Benditó G.. (2002). Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis. Nat. Neurosci. 5, 19– 26. 10.1038/nn783 11753414 · DOI
  133. Weber T. Zemelman B. V. McNew J. A. Westermann B. Gmachl M. Parlati F.. (1998). SNAREpins: minimal machinery for membrane fusion. Cell 92, 759– 772. 10.1016/s0092-8674(00)81404-x 9529252 · DOI
  134. Weimbs T. Low S. H. Chapin S. J. Mostov K. E. Bucher P. Hofmann K. (1997). A conserved domain is present in different families of vesicular fusion proteins: a new superfamily. Proc. Natl. Acad. Sci. U S A 94, 3046– 3051. 10.1073/pnas.94.7.3046 9096343 PMC20319 · DOI
  135. Wen P. J. Grenklo S. Arpino G. Tan X. Liao H.-S. Heureaux J.. (2016). Actin dynamics provides membrane tension to merge fusing vesicles into the plasma membrane. Nat. Commun. 7: 12604. 10.1038/ncomms12604 27576662 PMC5013665 · DOI
  136. Wesolowski J. Caldwell V. Paumet F. (2012). A novel function for SNAP29 (Synaptosomal-Associated Protein of 29 kDa) in mast cell phagocytosis. PLoS One 7: e49886. 10.1371/journal.pone.0049886 23185475 PMC3503860 · DOI
  137. Wightman R. M. Haynes C. L. (2004). Synaptic vesicles really do kiss and run. Nat. Neurosci. 7, 321– 322. 10.1038/nn0404-321 15048116 · DOI
  138. Winkle C. C. McClain L. M. Valtschanoff J. G. Park C. S. Maglione C. Gupton S. L. (2014). A novel Netrin-1-sensitive mechanism promotes local SNARE-mediated exocytosis during axon branching. J. Cell Biol. 205, 217– 232. 10.1083/jcb.201311003 24778312 PMC4003241 · DOI
  139. Wisco D. Anderson E. D. Chang M. C. Norden C. Boiko T. Fölsch H.. (2003). Uncovering multiple axonal targeting pathways in hippocampal neurons. J. Cell Biol. 162, 1317– 1328. 10.1083/jcb.200307069 14517209 PMC2173963 · DOI
  140. Wong S. H. Zhang T. Xu Y. Subramaniam V. N. Griffiths G. Hong W. (1998). Endobrevin, a novel synaptobrevin/VAMP-like protein preferentially associated with the early endosome. Mol. Biol. Cell 9, 1549– 1563. 10.1091/mbc.9.6.1549 9614193 PMC25382 · DOI
  141. Wu Z. Auclair S. M. Bello O. Vennekate W. Dudzinski N. R. Krishnakumar S. S.. (2016). Nanodisc-cell fusion: control of fusion pore nucleation and lifetimes by SNARE protein transmembrane domains. Sci. Rep. 6: 27287. 10.1038/srep27287 27264104 PMC4893671 · DOI
  142. Wu Z. Bello O. D. Thiyagarajan S. Auclair S. M. Vennekate W. Krishnakumar S. S.. (2017). Dilation of fusion pores by crowding of SNARE proteins. eLife 6: e22964. 10.7554/eLife.22964 28346138 PMC5404929 · DOI
  143. Yang L. Dun A. R. Martin K. J. Qiu Z. Dunn A. Lord G. J.. (2012). Secretory vesicles are preferentially targeted to areas of low molecular SNARE density. PLoS One 7: e49514. 10.1371/journal.pone.0049514 23166692 PMC3499460 · DOI
  144. Yu H. Liu Y. Gulbranson D. R. Paine A. Rathore S. S. Shen J. (2016). Extended synaptotagmins are Ca2-dependent lipid transfer proteins at membrane contact sites. Proc. Natl. Acad. Sci. 113, 4362– 4367. 10.1073/pnas.1517259113 27044075 PMC4843466 · DOI
  145. Yuan T. Lu J. Zhang J. Zhang Y. Chen L. (2015). Spatiotemporal detection and analysis of exocytosis reveal fusion “hotspots” organized by the cytoskeleton in endocrine cells. Biophys. J. 108, 251– 260. 10.1016/j.bpj.2014.11.3462 25606674 PMC4302205 · DOI
  146. Zheng J. Lamoureux P. Santiago V. Dennerll T. Buxbaum R. E. Heidemann S. R. (1991). Tensile regulation of axonal elongation and initiation. J. Neurosci. 11, 1117– 1125. 10.1523/jneurosci.11-04-01117.1991 2010807 PMC6575379 · DOI
  147. Zhou Q. Xiao J. Liu Y. (2000). Participation of syntaxin 1A in membrane trafficking involving neurite elongation and membrane expansion. J. Neurosci. Res. 61, 321– 328. 10.1002/1097-4547(20000801)61:3<321::aid-jnr10>3.0.co;2-l 10900079 · DOI
  148. Zylbersztejn K. Petkovic M. Burgo A. Deck M. Garel S. Marcos S.. (2012). The vesicular SNARE Synaptobrevin is required for Semaphorin 3A axonal repulsion. J. Cell Biol. 196, 37– 46. 10.1083/jcb.201106113 22213797 PMC3255983 · DOI

Cited by

Sorted by citations

Authors
Urbina, F. L., & Gupton, S. L.
Affiliations
University of North Carolina at Chapel Hill (US)
Corresponding author
Gupton, Stephanie L.
ORCID
Gupton, Stephanie L.
Venue
Frontiers in Molecular Neuroscience
Publisher
Frontiers Media SA
Published
2020-08-07
Volume
13
Pages
133-133
ISSN
1662-5099 (ISSN-L)
DOI
10.3389/fnmol.2020.00133
PMC
PMC7427632
OpenAlex
W3048280835
Cited by
48
References
5
Citations by year
2026: 7 · 2025: 9 · 2024: 7 · 2023: 8 · 2022: 8 · 2021: 8 · 2020: 1
FWCI
0.74
Type
journal article
Language
en
Open access
Licence
Locations
  • Frontiers in Molecular Neuroscience (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
National Institute of Neurological Disorders and Stroke (R01NS112326, F31NS103586)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Cellular transport and secretion
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Extracellular vesicles in disease
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neuroscience and Neuropharmacology Research
Keywords
SNARE proteins, exocytosis, neuronal development, membrane fusion, fusion pore, kiss-and-run, VAMP2, SNAP-25, syntaxin-1, neurite outgrowth, axon specification, synaptogenesis, fusion kinetics

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